Understanding the impact of agri-environment schemes on emerging infectious diseases in pollinators

The devastating spread of the Ebola virus in West Africa is one of many recent examples of emerging diseases that directly impact human health. However, emerging diseases in managed and wild animals may also indirectly affect human health and food security. For example, the global spread of a parasitic mite (called Varroa destructor), and the viruses it transmits, in honeybees has wiped out wild honeybee populations, and driven large declines in the number of managed hives in Europe and North America. As honeybees are important for pollinating crops and producing honey, such losses could have significant impacts on the sustainability of agricultural systems and, thus, through declines in food production, human health.

Pollination - the fertilization of flowers to produce seeds and fruit - is a key process in both agricultural and natural environments. While honeybees are important pollinators, wild bees, such as bumblebees, are just as, if not more important for both crops and wildflowers. Consequently, the fact that both honeybees and wild bees are in decline across much of the globe is a major concern. Earlier declines in bumblebees and other wild bees appeared to be driven by the loss of suitable habitat, containing the flowers, nesting sites, and hibernation sites needed for survival. However, recently, major declines in bumblebees in North and South America appear to be related to the spread of emerging pathogens. Thus, the discovery that the viruses driving declines in honeybees are also present in wild bumblebees is deeply worrying. Recent research in the UK has shown that harmful viruses like Deformed Wing Virus are being transmitted to-and-fro between managed honeybees and wild bumblebees. Such transmission may be exacerbated by the planting of nectar and pollen-producing flower strips, one of the major ways farmers try to enhance the populations of wild pollinators for crop pollination. However, we currently do not know the major direction of spread for these viruses - is it from honeybees to bumblebees, or vice versa? - and whether wild-flower strips change the rate and direction of transmission, or the actual mechanics behind how transmission occurs. If we are to manage emerging viral diseases in our essential managed and wild bees, these are the questions we need to address.

In our work, we propose to combine real-world and laboratory studies to answer these questions. First, we will sample bees from farms in areas with and without wild-flower strips, and screen them for viruses. We will use new genome sequencing technology, combined with complex statistical models, to determine whether viruses spread predominantly from honeybees to bumblebees, or vice versa, and whether the presence of wild-flower strips enhances transmission or changes its direction. In combination with this, we will conduct controlled experiments in the laboratory to determine how the type of flower and the length of time viral particles are on flowers, affect the likelihood of a flower-visiting bee becoming infected. This will help us to understand the fine-scale mechanisms by which transmission among bees takes place. Finally, we will conduct large experiments with whole hives of bees in polytunnels to test how the density of flowers, type of flowers, and density of bees determine the rate of viral spread. Together, these laboratory and semi-field (polytunnel) experiments will help us to understand the patterns of transmission found in wild bees from the first part of the project. Ultimately, we will use these results to make recommendations on how to reduce the transmission of emerging viruses among our wild and managed bees, and thus enhance their populations while maximising pollination of both crops and wildflowers in the UK landscape

Emerging diseases and the multi-host pathogens that cause them threaten animal and human health and can put ecosystem services at risk. Insect pollinators, particularly wild and managed bees, provide a key ecosystem service and are crucial for maintaining food security. But bees are in decline, and multiple lines of evidence suggest that emerging diseases may play a key role in these declines. Inter-specific transmission in pollinators is facilitated by niche overlap; sharing floral resources can promote indirect disease transmission. However, the provision of floral resources through agri-environment schemes is the key component in current programs to enhance pollinator assemblages for ecosystem services in agricultural landscapes.
Based on this landscape-scale experiment, we will study the fundamental ecology of disease transmission in this community to determine who and what drives transmission and how we can optimize management to reduce the risk of disease emergence. We will combine studying disease transmission dynamics in the field with targeted experiments to dissect the drivers of disease transmission in agricultural landscapes. We will first assess the full viral community of pollinators across conventional and enriched agricultural landscapes. Then we will determine the spatio-temporal source-sink dynamics of 3 key pollinator viral pathogens by using cutting-edge phylogenetic modelling to reconstruct transmission dynamics under conventional and enriched agricultural schemes. We will use lab-experiments to determine how time-lags, and floral complexity affect within- and between-species transmission. Informed by fieldwork and lab experiments, we will experimentally determine how transmission is mediated by floral resources and pollinator density in semi-natural enclosures. With these results, we will provide fundamental insights into the evolutionary ecology of emerging diseases and, ultimately, improved agricultural management schemes for pollinators.

This project will: (i) substantially enhance our understanding of the landscape of RNA viruses, both emerging and non-emerging, in wild and managed pollinators, (ii) determine the dynamics, directionality, and overall epidemiology of emerging diseases in wild and managed pollinators and test whether these are affected by agri-environment schemes, (iii) elucidate the mechanisms behind disease transmission and determine how they impact transmission at semi-field scales, and consequently (iv) provide suggestions for management of agri-environment schemes that are designed to benefit wild and commercial pollinator populations, in order to minimize the threat of emerging disease. In addition to the academic community (see 'academic beneficiaries'), we have identified 5 sectors that will benefit from this work. We aim for rapid and high impact of our results on policy for pollinator management, enhancing the UK's biodiversity and agri-economy.

1) national and international policy-makers, regulators & government
Emerging disease is a significant focus of attention for national and EU-level policy makers, e.g., the designation of notifiable diseases and requirement for health certificates prior to international bee transport. Policy makers and government will benefit from this work as it will fill a major hole in our understanding of whether and how viruses emerge across the commercial-wild pollinator divide, as well as the impact of agri-environmental schemes on this emergence. This is critical during the ongoing development and implementation in the UK of the reformed Common Agricultural Policy and the National Pollinator Strategies, as well as the development of new agri-environment schemes. Consequently, our outputs will enable the development of evidence-based policy to protect the ecosystem service of pollination.

2) land management and seed producers
Agri-environment schemes aim to improve ecosystem services and conservation. To achieve this for pollinators, seed producers that provide nectar and pollen seed mixtures and land managers need to understand how these schemes affect not only pollinator abundance and diversity, but also how they affect pollinator health. Our results will allow seed producers to optimize the seed mixtures they sell and will allow land managers to improve pollination services and pollinator conservation.

3) conservation agencies
Numerous conservation NGOs in the UK (e.g., Bumblebee Conservation Trust, Buglife, Bee Guardian Foundation, RSPB) and globally (IUCN) require a deeper understanding of the factors driving wild pollinator declines in order to devise both policy and on-the-ground management. Our research will provide the information necessary to enable such agencies to manage both floral interventions and commercial honeybees, to maximise the health of wild pollinator populations

4) commercial honeybee managers
Currently, over 40,000 honeybee colonies are managed commercially in the UK, for pollination services and honey production. Our research results will enable commercial producers to minimize both the impacts of emerging diseases spreading from managed honeybees into wild bees, and the likelihood of acquiring such diseases from the wild, which will therefore increase the value and efficiency of these important commercial pollinators.

5) publics
From specialist interest groups, such as Beekeeping Associations, through to schools and adult communities, there is a deep and abiding interest in bees and their health. Results from our work will be of broad interest to this range of public communities, enabling them to understand how science is trying to address the global problem of bee decline. Moreover, our results will have a direct and immediate role in conserving pollinators, as urban gardens are currently important refuges for these beneficial insects due to their forage availability. Our research results may directly benefit the design of bee-friendly gardening schemes